Eusociality and the transition from biparental to alloparental care in termites

Abstract

1. In eusocial organisms, cooperative brood care within a colony represents a situation where the ancestral parental care duties have shifted away from the reproductive parent(s) towards their offspring. The shift to alloparental care was often instrumental in the initial emergence of eusociality, as it ultimately contributed to the establishment of the reproductive division of labour.2. Remarkably, eusocial taxa such as ants and termites, which still display an ancestral independent colony foundation phase, must go through an obligatory parental care period, as a temporary subsocial family unit. In termites specifically, an incipient colony inherently remains a woodroach family unit until alloparental care is established. Colony foundation success can then be limited by a series of factors that may include environmental, behavioural, symbiotic and physiological constraints.3. In this study, 450 incipient termite colonies (Coptotermes gestroi) were established to investigate the timing of physiological changes in founders during the transition from biparental to alloparental care. Results showed that the finite initial internal nutritional resources that alates carry during the dispersal flight are a primary limiting factor for successful colony establishment. The Coptotermes queen and king must rapidly establish (<150 days) their first cohort of offspring to reach alloparental care or simply run out of resources and die. Alates, therefore, carry just enough internal resources to produce the first few alloparents (< 15 workers) to prime the system towards colony ergonomic growth, with a definitive shift to solely reproductive functions. 4. Eusocial insect primary reproductive traits were optimized for three successive functions within the life cycle of a colony: alate dispersal (sexual reproduction), colony foundation (parental care) and colony growth (increased egg production towards colony maturity). However, results suggest that trade-offs involving these functions appear to primarily favour dispersal ones (quantity vs. quality of alates), as founder(s) carry minimal resources and have no room for parental care inefficiency and as they then fully rely on their alloparents for further reproductive output.

King- and queen-specific degradation of uric acid contributes to reproduction in termites

“…In addition, the differences in expressions of genes associated with purine catabolism among alates, young and old reproductives indicate a shift in metabolism at a different part of the life of kings and queens. This fits with the observation in previous studies, where the king and queen founding a colony need to provide their internal nitrogen resources to their first brood, but once established with workers, the dynamic nitrogen flows within the colony changes [59][60][61].…”

Succession of the microbiota in the gut of reproductives of Macrotermes subhyalinus (Termitidae) at colony foundation gives insights into symbionts transmission

“…The absence of sexual dimorphism on the microbiota was consistently observed on protozoan communities of lower termites during the first months of colony foundation (Shimada et al, 2013;Michaud et al, 2020), suggesting that both sexes are similarly involved in feeding tasks at this stage. This involvement of both parents (biparental care) was demonstrated in several studies on lower termites (Shimada et al, 2013;Benjamino and Graf, 2016;Inagaki et al, 2020;Velenovsky et al, 2021;Chouvenc, 2022) and very recently on Macrotermes natalensis (Sinotte et al, 2022) and was likely inherited from the common ancestor of termites (Nalepa, 2015).…”

“…The increase in the gut size (Shimada et al, 2013) or relative weight (Nalepa et al, 2001) seems common during the first period of colony foundations in lower termites. The enlargement of the gut seems to be aligned with a gain in wet weight of reproductives during this period (Nalepa et al, 2001;Chouvenc, 2022). However, the dry body weight and the content in nutritional reserves decrease at the same time (Johnston and Wheeler, 2007;Chouvenc, 2022), likely indicating that the increase of the gut size in dealates reflects the rehydration of the gut, rather than the feeding behavior only.…”

“…The enlargement of the gut seems to be aligned with a gain in wet weight of reproductives during this period (Nalepa et al, 2001;Chouvenc, 2022). However, the dry body weight and the content in nutritional reserves decrease at the same time (Johnston and Wheeler, 2007;Chouvenc, 2022), likely indicating that the increase of the gut size in dealates reflects the rehydration of the gut, rather than the feeding behavior only. Albeit most of studies assessing the feeding behavior concern lower termites, the engorgement of dealates during the first weeks of colony foundation may be ubiquitous and can be a component of the observed enlargement of the gut in the current study.…”

Sandwich Tern Feeds Juvenile on Wintering Grounds in Southern Namibia

“…Gittleman 1981, Gans 1996, Trumbo 2012), whilst many taxa show some form of care for their young (e.g. Clapham 1996, Balshine-Earn & Earn 1998, Schreiber & Burger 2001, Ringler et al 2013, Chouvenc 2022). The duration of parental care varies widely among organisms (e.g Gonzalez-Vojer & Kohm 2010…”